Autotrophic growth of nitrifying community in an agricultural soil

ISME Journal

Volumn 5, Issue 7, 2011, Pages 1226-1236

  Xia, Weiwei ^a,b   Zhang, Caixia ^c   Zeng, Xiaowei ^d   Feng, Youzhi ^a   Weng, Jiahua ^a   Lin, Xiangui ^a   Zhu, Jianguo ^a   Xiong, Zhengqin ^c   Xu, Jian ^d   Cai, Zucong ^a   Jia, Zhongjun ^a  

^a INSTITUTE OF SOIL SCIENCE   (China)

^b UNIVERSITY OF CHINESE ACADEMY OF SCIENCES   (China)

^c NANJING AGRICULTURAL UNIVERSITY   (China)

^d QINGDAO INSTITUTE OF BIOENERGY AND BIOPROCESS TECHNOLOGY   (China)

Author keywords

agricultural soil; ammonia oxidizing archaea; ammonia oxidizing bacteria; nitrite oxidizing bacteria; pyrosequencing; stable isotope probing

Indexed keywords

AMMONIA; NITRITE;

AGRICULTURAL SOIL; AUTOTROPHY; GROWTH RATE; MICROBIAL COMMUNITY; MICROCOSM; PHYLOGENETICS; PROBE; PROKARYOTE; STABLE ISOTOPE; THERMOPHILIC BACTERIUM;

AGRICULTURE; ARCHAEAL GENE; ARCHAEBACTERIUM; ARTICLE; AUTOTROPHY; BACTERIAL GENE; BACTERIUM; CLASSIFICATION; DNA SEQUENCE; GENE LIBRARY; GENETICS; GROWTH, DEVELOPMENT AND AGING; HIGH THROUGHPUT SEQUENCING; METABOLISM; MICROBIOLOGY; NITRIFICATION; PHYLOGENY; RNA GENE; SOIL;

AGRICULTURE; AMMONIA; ARCHAEA; AUTOTROPHIC PROCESSES; BACTERIA; GENE LIBRARY; GENES, ARCHAEAL; GENES, BACTERIAL; GENES, RRNA; HIGH-THROUGHPUT NUCLEOTIDE SEQUENCING; NITRIFICATION; NITRITES; PHYLOGENY; SEQUENCE ANALYSIS, DNA; SOIL; SOIL MICROBIOLOGY;

ARCHAEA; BACTERIA (MICROORGANISMS); NITROBACTER; NITROSOMONADALES; NITROSOSPIRA; NITROSPIRA;

EID: 79959596861     PISSN: 17517362     EISSN: 17517370     Source Type: Journal    
DOI: 10.1038/ismej.2011.5     Document Type: Article

References (57)

1. Agogue H, Brink M, Dinasquet J, Herndl GJ. (2008).Major gradients in putatively nitrifying and nonnitrifying Archaea in the deep North Atlantic. Nature 456: 788-791.
2. Alawi M, Lipski A, Sanders T, Eva Maria P, Spieck E. (2007). Cultivation of a novel cold-adapted nitrite oxidizing betaproteobacterium from the Siberian Arctic. ISME J 1: 256-264. (Pubitemid 47145296)
3. Alawi M, Off S, Kaya M, Spieck E. (2009). Temperature influences the population structure of nitrite-oxidizing bacteria in activated sludge. Environ Microbiol Rep 1: 184-190.
4. Attard E, Poly F, Commeaux C, Laurent F, Terada A, Smets BF et al. (2010). Shifts between nitrospira- and nitrobacter-like nitrite oxidizers underlie the response of soil potential nitrite oxidation to changes in tillage practices. Environ Microbiol 12: 315-326.
5. Bock E,Wagner M. (2006). Oxidation of inorganic nitrogen compounds as an energy source. In: Dworkin M, Falkow S (eds). The Prokaryotes. Springer Verlag: New York, pp 457-495.
6. Brochier-Armanet C, Boussau B, Gribaldo S, Forterre P. (2008). Mesophilic crenarchaeota: Proposal for a third archaeal phylum, the Thaumarchaeota. Nat Rev Microbiol 6: 245-252. (Pubitemid 351256319)
7. Chen Y, Wu L, Boden R, Hillebrand A, Kumaresan D, Moussard H et al. (2009). Life without light: Microbial diversity and evidence of sulfur- and ammonium-based chemolithotrophy in Movile Cave. ISME J 3: 1093-1104.
8. Chu H, Fujii T, Morimoto S, Lin X, Yagi K, Hu J et al. (2007). Community structure of ammonia-oxidizing bacteria under long-term application of mineral fertilizer and organic manure in a sandy loam soil.Appl Environ Microbiol 73: 485-491. (Pubitemid 46147578)
9. Cole JR, Wang Q, Cardenas E, Fish J, Chai B, Farris RJ et al. (2009). The ribosomal database project: Improved alignments and new tools for rRNA analysis. Nucleic Acids Res 37: D141-D145.
10. Daims H, Nielsen JL, Nielsen PH, Schleifer K-H, Wagner M. (2001). In situ characterization of nitrospira-like nitrite-oxidizing bacteria active in wastewater treatment plants. Appl Environ Microbiol 67: 5273-5284. (Pubitemid 33701300)
11. de la Torre JR, Walker CB, Ingalls AE, Konneke M, Stahl DA. (2008). Cultivation of a thermophilic ammonia oxidizing archaeon synthesizing crenarchaeol.Environ Microbiol 10: 810-818. (Pubitemid 351160920)
12. DeLong E. (1992). Archaea in coastal marine environments.Proc Natl Acad Sci USA 89: 5685-5689.
13. Di HJ, Cameron KC, Shen JP, Winefield CS, O' Callaghan M, BOWATTE S et al. (2009). Nitrification driven by bacteria and not archaea in nitrogen rich grassland soils. Nat Geosci 2: 621-624.
14. Ehrich S, Behrens D, Lebedeva E, Ludwig W, Bock E. (1995). A new obligately chemolithoautotrophic, nitrite-oxidizing bacterium, Nitrospira moscoviensis sp. nov. and its phylogenetic relationship. Arch Microbiol 164: 16-23.
15. Erguder TH, Boon N, Wittebolle L, Marzorati M, Verstraete W. (2009). Environmental factors shaping the ecological niches of ammonia-oxidizing archaea.FEMS Microbiol Rev 33: 855-869.
16. Feliatra F, Bianchi M. (1993). Rates of nitrification and carbon uptake in the Rhone River plume (northwestern Mediterranean Sea). Microb Ecol 26: 21-28. (Pubitemid 24430215)
17. Francis CA, Roberts KJ, Beman JM, Santoro AE, Oakley BB. (2005). Ubiquity and diversity of ammonia-oxidizing archaea in water columns and sediments of the ocean. Proc Natl Acad Sci USA 102: 14683-14688. (Pubitemid 41457116)
18. Freitag TE, Chang L, Clegg CD, Prosser JI. (2005). Influence of inorganic nitrogen management regime on the diversity of nitrite-oxidizing bacteria in Agricultural Grassland Soils. Appl Environ Microbiol 71: 8323-8334. (Pubitemid 41803960)
19. Freitag TE, Chang L, Prosser JI. (2006). Changes in the community structure and activity of betaproteobacterial ammonia-oxidizing sediment bacteria along a freshwater-marine gradient. Environ Microbiol 8: 684-696. (Pubitemid 43363325)
20. Gruber N, Galloway JN. (2008). An earth-system perspective of the global nitrogen cycle. Nature 451: 293-296.
21. Gubry-Rangin C, Nicol GW, Prosser JI. (2010). Archaea rather than bacteria control nitrification in two agricultural acidic soils. FEMS Microbiol Ecol 74: 566-574.
22. Hatzenpichler R, Lebedeva EV, Spieck E, Stoecker K, Richter A, Daims H et al. (2008). A moderately thermophilic ammonia-oxidizing crenarchaeote from a hot spring. Proc Natl Acad Sci USA 105: 2134-2139. (Pubitemid 351439477)
23. Hovanec T, DeLong E. (1996). Comparative analysis of nitrifying bacteria associated with freshwater and marine aquaria. Appl Environ Microbiol 62: 2888-2896. (Pubitemid 26417349)
24. Hovanec TA, Taylor LT, Blakis A, Delong EF. (1998).Nitrospira-like bacteria associated with nitrite oxidation in freshwater aquaria. Appl Environ Microbiol 64: 258-264. (Pubitemid 28040323)
25. Huang WE, Ferguson A, Singer AC, Lawson K, Thompson IP, Kalin RM et al. (2009). Resolving genetic functions within microbial populations: In situ analyses using rRNA and mRNA stable isotope probing coupled with single-cell Raman-fluorescence in situ hybridization.Appl Environ Microbiol 75: 234-241.
26. 2- labeling studies of the de novo synthesis of polypeptides by Nitrosomonas europaea during recovery from acetylene and light inactivation of ammonia monooxygenase. J Biol Chem 267: 1534-1545.
27. Jia ZJ, Conrad R. (2009). Bacteria rather than Archaea dominate microbial ammonia oxidation in an agricultural soil. Environ Microbiol 11: 1658-1671.
28. Jiang H, Huang Q, Dong H, Wang P, Wang F, Li W et al. (2010). RNA-based investigation of ammonia-oxidizing archaea in Hot Springs of Yunnan Province, China.Appl Environ Microbiol 76: 4538-4541.
29. Könneke M, Bernhard AE, de la Torre JR, Walker CB, Waterbury JB, Stahl DA. (2005). Isolation of an autotrophic ammonia-oxidizing marine archaeon.Nature 437: 543-546. (Pubitemid 41613550)
30. Koops HP, Pommerening-Röser A. (2001). Distribution and ecophysiology of the nitrifying bacteria emphasizing cultured species. FEMS Microbiol Ecol 37: 1-9. (Pubitemid 32800676)
31. Koops HP, Purkhold U, Pommerening-Roser A, Timmermann G, Wagner M. (2006). The lithoautotrophic ammonia-oxidizing bacteria. In: Dworkin M, Falkow S (eds). The Prokaryotes. Springer Verlag: New York, pp 778-811.
32. Kowalchuk GA, Stephen JR. (2001). Ammonia-oxidizing bacteria: A model for molecular microbial ecology.Annl Rev Microbiol 55: 485-529. (Pubitemid 32978114)
33. Kumar S, Tamura K, Nei M. (2004). MEGA3: Integrated software for molecular evolutionary genetics analysis and sequence alignment. Brief Bioinform 5: 150-163.
34. Lam P, Jensen MM, Lavik G, McGinnis DF, Muller B, Schubert CJ et al. (2007). Linking crenarchaeal and bacterial nitrification to anammox in the Black Sea.Proc Natl Acad Sci USA 104: 7104-7109. (Pubitemid 47186016)
35. Lane DJ. (1991). 16S/23S rRNA sequencing. In: Stackebrandt E, Goodfellow M (eds). Nucleic Acid Techniques in Bacterial Systematics. John Wiley and Sons: New York, USA, pp 177-203.
36. Leininger S, Urich T, Schloter M, Schwark L, Qi J, Nicol GW et al. (2006). Archaea predominate among ammonia-oxidizing prokaryotes in soils. Nature 442: 806-809. (Pubitemid 44258909)
37. Lueders T, Manefield M, Friedrich MW. (2004). Enhanced sensitivity of DNA- and rRNA-based stable isotope probing by fractionation and quantitative analysis of isopycnic centrifugation gradients. Environ Microbiol 6: 73-78. (Pubitemid 38162029)
38. Martens-Habbena W, Berube PM, Urakawa H, de la Torre JR, Stahl DA. (2009). Ammonia oxidation kinetics determine niche separation of nitrifying Archaea and Bacteria. Nature 461: 976-979.
39. Meng L, Ding W, Cai Z. (2005). Long-term application of organic manure and nitrogen fertilizer on N2O emissions, soil quality and crop production in a sandy loam soil. Soil Biol Biochem 37: 2037-2045. (Pubitemid 41531237)
40. Mertens J, Broos K, Wakelin SA, Kowalchuk GA, Springael D, Smolders E. (2009). Bacteria, not archaea, restore nitrification in a zinc-contaminated soil. ISME J 3: 916-923.
41. Neufeld JD, Vohra J, Dumont MG, Lueders T, Manefield M, Friedrich MW et al. (2007). DNA stable-isotope probing. Nat Protocols 2: 860-866. (Pubitemid 46745584)
42. Nicol GW, Leininger S, Schleper C, Prosser JI. (2008). The influence of soil pH on the diversity, abundance and transcriptional activity of ammonia oxidizing archaea and bacteria. Environ Microbiol 10: 2966-2978.
43. Off S, Alawi M, Spieck E. (2010). Enrichment and physiological characterization of a novel nitrospiralike bacterium obtained from a marine sponge. Appl Environ Microbiol 76: 4640-4646.
44. Offre P, Prosser JI, Nicol GW. (2009). Growth of ammoniaoxidizing archaea in soil microcosms is inhibited by acetylene. FEMS Microbiol Ecol 70: 99-108.
45. Okano Y, Hristova KR, Leutenegger CM, Jackson LE, Denison RF, Gebreyesus B et al. (2004). Application of real-time PCR to study effects of ammonium on population size of ammonia-oxidizing bacteria in soil.Appl Environ Microbiol 70: 1008-1016. (Pubitemid 38568227)
46. Poly F, Wertz S, Brothier E, Degrange V. (2008). First exploration of nitrobacter diversity in soils by a PCR cloning-sequencing approach targeting functional gene nxrA. FEMS Microbiol Ecol 63: 132-140. (Pubitemid 350233286)
47. Reigstad LJ, Richter A, Daims H, Urich T, Schwark L, Schleper C. (2008). Nitrification in terrestrial hot springs of Iceland and Kamchatka. FEMS Microbiol Ecol 64: 167-174. (Pubitemid 351533426)
48. Rotthauwe J, Witzel K, Liesack W. (1997). The ammonia monooxygenase structural gene amoA as a functional marker: Molecular fine-scale analysis of natural ammonia- oxidizing populations. Appl Environ Microbiol 63: 4704-4712. (Pubitemid 27524201)
49. Santoro AE, Casciotti KL, Francis CA. (2010). Activity, abundance and diversity of nitrifying archaea and bacteria in the central California current. Environ Microbiol 12: 1989-2006.
50. Schleper C. (2010). Ammonia oxidation: Different niches for bacteria and archaea? ISME J 4: 1092-1094.
51. Schloss PD, Westcott SL, Ryabin T, Hall JR, Hartmann M, Hollister EB et al. (2009). Introducing mothur: Open-source, platform-independent, community-supported software for describing and comparing microbial communities. Appl Environ Microbiol 75: 7537-7541.
52. Schramm A, de Beer D, Wagner M, Amann R. (1998).Identification and activities in situ of nitrosospira and nitrospira spp. as dominant populations in a nitrifying fluidized bed reactor. Appl Environ Microbiol 64: 3480-3485. (Pubitemid 28411476)
53. Spang A, Hatzenpichler R, Brochier-Armanet C, Rattei T, Tischler P, Spieck E et al. (2010). Distinct gene set in two different lineages of ammonia-oxidizing archaea supports the phylum thaumarchaeota. Trends Microbiol 18: 331-340.
54. Treusch AH, Leininger S, Kletzin A, Schuster SC, Klenk H-P, Schleper C. (2005). Novel genes for nitrite reductase and Amo-related proteins indicate a role of uncultivated mesophilic crenarchaeota in nitrogen cycling. Environ Microbiol 7: 1985-1995. (Pubitemid 41752386)
55. Wagner M, Rath G, Koops H-P, Flood J, Amann R. (1996).In situ analysis of nitrifying bacteria in sewage treatment plants. Water Sci Technol 34: 237-244. (Pubitemid 26329006)
56. 13C incorporation into DNA as a means of identifying the active components of ammonia-oxidizer populations. Lett Appl Microbiol 32: 398-401. (Pubitemid 32521333)
57. Zhang LM, Offre PR, He JZ, Verhamme DT, Nicol GW, Prosser JI. (2010). Autotrophic ammonia oxidation by soil thaumarchaea. Proc Natl Acad Sci USA 107: 17240-17245.